Sex Differences in Rhesus Monkeys’ Digit Ratio (2D:4D Ratio) and Its Association With Maternal Social Dominance Rank

Abstract

Prenatal androgen exposure (PAE) plays a pivotal role in masculinizing the developing body and brain, and extreme exposure may contribute to autism, anxiety disorder and schizophrenia. One commonly used biomarker for PAE is the pointer-to-ring-finger digit length (2D:4D) ratio. Although this biomarker is widely used in human studies, relatively few studies have investigated 2D:4D ratio in nonhuman primates, particularly rhesus macaques (Macaca mulatta), one of the most commonly used animals in biomedical research. Thus far, data suggest that sexual dimorphism in 2D:4D ratio may be in the opposite direction in some monkey species, when compared to the pattern exhibited by humans and great apes. Using a large sample size, we investigated whether rhesus monkeys’ 2D:4D ratio shows the same sex-differentiated pattern present in other Old World monkey species. We also investigated whether individual differences in 2D:4D ratio are associated with the social dominance rank of subjects’ mothers during pregnancy, and the social dominance rank the subjects attained as adults. Subjects were 335 rhesus monkeys between 3 years and 24 years of age (M = 6.6). Maternal dominance rank during pregnancy and subjects’ adult dominance rank were categorized into tertiles (high, middle and low). Results showed that, across both hands, male rhesus monkeys exhibited higher 2D:4D ratio than females, a pattern consistent with other monkey species and a reversal from the pattern typically observed in humans and apes. This sex difference was modulated by maternal dominance rank, with female offspring of high-ranking and middle-ranking mothers exhibiting masculinized 2D:4D ratio, indicating that maternal dominance rank during pregnancy may influence levels of PAE. There was no association between subjects’ 2D:4D ratio and the social dominance rank they attained as adults. These findings show a consistent sex difference in Old World monkeys’ 2D:4D ratio that diverges from the pattern observed in apes and humans, and suggest maternal social dominance rank modulates PAE in rhesus monkeys.

Anogenital distance as a measure of male competitive ability in Rwenzori Angolan colobus

“…Similar results have been shown for female dominance rank in non‐human primates, with PAE assessed using digit ratios as a biomarker. For rhesus macaques ( M. mulatta ; Nelson et al, 2010), Hamadryas baboons ( P. hamadryas ; Howlett et al, 2012), and chacma baboons ( P. ursinus ,; Howlett et al, 2012, 2015) high female dominance rank was correlated with what was thought to be a more masculinized 2D:4D ratio and therefore greater PAE (but see Baxter et al, 2018 for a different interpretation of digit ratios in M. mulatta ). In rhesus macaques, PAE leading to higher dominance rank was most pronounced among related females within matrilines, consistent with the fact that day‐to‐day competitive interactions occur most frequently between closely ranked kin (Nelson et al, 2010).…”

“…In rhesus macaques, PAE leading to higher dominance rank was most pronounced among related females within matrilines, consistent with the fact that day‐to‐day competitive interactions occur most frequently between closely ranked kin (Nelson et al, 2010). Dominance rank for female macaques and chacma baboons is maternally inherited, thus the maternal gestational environment and PAE experienced by the fetus are likely related to the mother's experiences within the hierarchy (Baxter et al, 2018; Howlett et al, 2015; Nelson et al, 2010). Indeed, in some wild mammal species, high‐ranking mothers have been shown to experience higher levels of testosterone than lower‐ranking mothers, which could influence PAE for offspring (e.g., Papio sp.…”

“…A growing body of research utilizing 2D:4D digit ratios suggests that PAE are important in contributing to variation in many behavioral, cognitive, and psychological traits in humans (reviewed in Fink, Manning, & Neave, 2004; Teatero & Netley, 2013; Turanovic, Pratt, & Piquero, 2017; Valla & Ceci, 2011) and non‐human primates (Howlett et al, 2012, 2015; Nelson & Shultz, 2010; Nelson et al, 2010). For most animal species however: (a) measurement of digit ratio is impossible (i.e., no digits) or impractical, (b) the associations between PAE and digit ratios have not been made, (c) some digits may grow postnatally (Hampson & Sankar, 2012; McIntyre, Cohn, & Ellison, 2006), (d) one hand may be more affected by PAE than the other (Abbott et al, 2012), and (e) the ratio may be opposite to expectations (i.e., Baxter et al, 2018; Roney et al, 2004). We, therefore, suggest that AGD is a better measure for PAE in wild animals and should be explored thoroughly in a range of species and taxa for its potential as a widely applicable metric to examine within‐ and between‐sex variability.…”

“…PAE and its effects on female dominance have been assessed in a few other non‐human primates using the 2D:4D ratio (i.e., the ratio of length between the second and fourth digit on the hand) as a biomarker. 2D:4D ratios are sexually dimorphic, being smaller in males than females in many species (Baxter, Wood, Witczak, Bales, & Higley, 2019; Galis, Ten Broek, Van Dongen, & Wijnaendts, 2010; Manning, Bundred, Newton, & Flanigan, 2003; McIntyre et al, 2009; but see: Baxter et al, 2018; Roney et al, 2004). In captive ( Papio hamadryas , Papio ursinus ; Howlett, Marshall, & Hughes, 2012), wild ( P. ursinus ; Howlett, Setchell, Hill, & Barton, 2015), and semifree ranging ( M. mulatta ; Nelson, Hoffman, Gerald, & Shultz, 2010) non‐human primates, masculinized 2D:4D ratios in females have been shown to be associated with higher female dominance rank.…”

“…This effect of PAE on adult dominance is likely due to the organizational effects of androgens on the developing brain, which later increases the likelihood of aggressive behaviors that maintain dominance (e.g., non‐human primates, Knickmeyer & Baron‐Cohen, 2006; Nelson et al, 2010; Wallen, 1996, 2005; humans, Bailey & Hurd, 2005; Manning & Fink, 2008; Neave, Laing, Fink, & Manning, 2003; van der Meij, Almela, Buunk, Dubbs, & Salvador, 2012). However, 2D:4D ratio may be misleading as a biomarker for PAE since one hand may be more affected than the other (Abbott et al, 2012) and there are species differences in how the ratio is expressed in males versus females (Baxter et al, 2018; Roney et al, 2004).…”